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Current Topics in Phytochemistry   Volumes    Volume 2 
Cyclic nucleotides and signal transduction in higher plants
Gideon Polya
Pages: 51 - 67
Number of pages: 17
Current Topics in Phytochemistry
Volume 2 

Copyright © 1999 Research Trends. All rights reserved

The cyclic nucleotides 3’,5’-cyclic GMP (cGMP) and 3’,5’-cyclic AMP (cAMP) have critical functions in animal and fungal cell signal transduction, the cytosolic levels of these so-called “second messengers” rising transiently in response to particular external hormonal and other signals and then falling through the action of cyclic nucleotide phosphodiesterases. The second messengers cAMP and cGMP act, respectively, by opening cAMP- or cGMP- gated ion channels or by activating cAMP-dependent protein kinase (PKA) or cGMP-dependent protein kinase (PKG) and, in addition, a cAMP receptor in Dictyostelium has a key developmental paracrine signal transduction function. May possible elements of a cyclic nucleotide regulatory system have been found in plants including cAMP, cGMP, adenylate cyclase, guanylate cyclase, cyclic nucleotide-hydrolyzing phosphodiesterases and a number of cyclic nucleotide-binding proteins. While analogues/homologues of PKA or PKG have not been found in plants, proteins homologous to the cyclic nucleotide-gated ion channels of other eukaryotes are present in higher plants. An Arabidopsis gene GCRI encodes a putative seven transmembrane element receptor-like protein with similarity to the Dictyostelium cAMP receptor protein. Stomatal opening clearly involves cGMP, which is also involved in light-regulated, phytochrome-mediated gene transcription in plants and has been implicated, together with cyclic adenosine 5’-diphosphate ribose (cADPR), in plant defense gene induction. Microinjection experiments involving ADP-ribosyl cyclase and cADPR have implicated cADPR in abscisic acid (ABA)-induced gene expression involving cADPR-induced Ca2+ release as an intermediate signal transduction step. Stomatal opening can be induced by animal atrial natriuretic peptide (ANP), this induction being inhibited by particular guanylate cyclase inhibitor. A plant peptide that cross-reacts with antibodies to ANP also induces stomatal opening and increases cGMP in gibberellic acid (GA)-induced α-amylase expression in barley aleurone has been suggested from GA-induced elevation of cGMP that is inhibited by a guanylate cyclase inhibitor that also inhibits GA-induced α-amylase expression. Defense gene expression in tobacco is induced by cGMP and cADPR and the levels of cGMP are increased by treatments elevating NO concentration in tobacco leaves. Whole plant cell patch clamp and microinjection experiments have shown that plant cell outward K+ channel activity is stimulated by cAMP and by PKA catalytic subunit and inhibited by the PKA inhibitor protein (PKI). A transient peak of cAMP content is observed during the S and G1 phases of the cell cycle in tobacco cells that can be abolished by indomethacin, an inhibitor of mitosis in both plant and animal cells and an inhibitor of prostaglandin synthesis in animal systems. Several plant proteins have similarities to the animal nuclear transcription factor CREB proteins that bind to the cAMP response element (CRE). A number of plant proteins are phosphorylated in vitro by PKA and other experiments also point to the possibility of plant protein kinases with substrate specificities overlapping those of PKA. Representatives of many classes of plant defensive secondary metabolities are potent inhibitors of PKA, an enzyme which is involved in “hunger” responses of animals and fungi that consume plants and which is critically involved in fungal pathogen invasion of higher plants. A substantial body of molecular evidence has now accumulated that is consistent with a regulatory function for cyclic nucleotides in plant signal transduction, the evidence for such a role for cGMP being particularly convincing.
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